Literature DB >> 21327075

Dynamic properties of meiosis-specific lamin C2 and its impact on nuclear envelope integrity.

Daniel Jahn1, Sabine Schramm, Ricardo Benavente, Manfred Alsheimer.   

Abstract

A hallmark of meiosis is the precise pairing and the stable physical connection (synapsis) of the homologous chromosomes. These processes are essential prerequisite for their proper segregation. Pairing of the homologs during meiotic prophase I critically depends on characteristic movements of chromosomes. These movements, in turn, require attachment of meiotic telomeres to the nuclear envelope and their subsequent dynamic repositioning. Dynamic repositioning of meiotic telomeres goes along with profound structural reorganization of the nuclear envelope. The short A-type lamin C2 is thought to play a critical role in this process due to its specific expression during meiotic prophase I and the unique localization surrounding telomere attachments. Consistent with this notion, here we provide compelling evidence that meiosis-specific lamin C2 features a significantly increased mobility compared to somatic lamins as revealed by photobleaching techniques. We show that this property can be clearly ascribed to the lack of the N-terminal head and the significantly shorter α-helical coil domain. Moreover, expression of lamin C2 in somatic cells induces nuclear deformations and alters the distribution of the endogenous nuclear envelope proteins lamin B1, LAP2, SUN1 and SUN2. Together, our data define lamin C2 as a "natural lamin deletion mutant" that confers unique properties to the nuclear envelope which would be essential for dynamic telomere repositioning during meiotic prophase I.

Entities:  

Keywords:  A-type lamins; germ cells; lamin C2; meiosis; nuclear envelope; nuclear lamina; spermatocytes; spermatogenesis

Mesh:

Substances:

Year:  2010        PMID: 21327075      PMCID: PMC3027034          DOI: 10.4161/nucl.1.3.11800

Source DB:  PubMed          Journal:  Nucleus        ISSN: 1949-1034            Impact factor:   4.197


  62 in total

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Journal:  J Biol Chem       Date:  2006-07-05       Impact factor: 5.157

2.  Transmembrane protein Sun2 is involved in tethering mammalian meiotic telomeres to the nuclear envelope.

Authors:  Johannes Schmitt; Ricardo Benavente; Didier Hodzic; Christer Höög; Colin L Stewart; Manfred Alsheimer
Journal:  Proc Natl Acad Sci U S A       Date:  2007-04-23       Impact factor: 11.205

3.  Gene structure and chromosomal localization of the murine lamin B2 gene.

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Journal:  Eur J Cell Biol       Date:  1991-12       Impact factor: 4.492

4.  The CaaX motif of lamin A functions in conjunction with the nuclear localization signal to target assembly to the nuclear envelope.

Authors:  D Holtz; R A Tanaka; J Hartwig; F McKeon
Journal:  Cell       Date:  1989-12-22       Impact factor: 41.582

Review 5.  The nuclear envelope.

Authors:  E A Nigg
Journal:  Curr Opin Cell Biol       Date:  1989-06       Impact factor: 8.382

6.  The role of the head and tail domain in lamin structure and assembly: analysis of bacterially expressed chicken lamin A and truncated B2 lamins.

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Journal:  J Struct Biol       Date:  1992 Jan-Feb       Impact factor: 2.867

7.  Expression in Escherichia coli of human lamins A and C: influence of head and tail domains on assembly properties and paracrystal formation.

Authors:  R D Moir; A D Donaldson; M Stewart
Journal:  J Cell Sci       Date:  1991-06       Impact factor: 5.285

8.  The CaaX motif is required for isoprenylation, carboxyl methylation, and nuclear membrane association of lamin B2.

Authors:  G T Kitten; E A Nigg
Journal:  J Cell Biol       Date:  1991-04       Impact factor: 10.539

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Authors:  G Krohne; I Waizenegger; T H Höger
Journal:  J Cell Biol       Date:  1989-11       Impact factor: 10.539

10.  Differential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: a developmental study.

Authors:  R A Röber; K Weber; M Osborn
Journal:  Development       Date:  1989-02       Impact factor: 6.868

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  10 in total

1.  Pushing the (nuclear) envelope into meiosis.

Authors:  Abby F Dernburg
Journal:  Genome Biol       Date:  2013-03-27       Impact factor: 13.583

Review 2.  Diseases of the Nucleoskeleton.

Authors:  James M Holaska
Journal:  Compr Physiol       Date:  2016-09-15       Impact factor: 9.090

Review 3.  Structural and functional adaptations of the mammalian nuclear envelope to meet the meiotic requirements.

Authors:  Jana Link; Daniel Jahn; Manfred Alsheimer
Journal:  Nucleus       Date:  2015-02-12       Impact factor: 4.197

4.  Repression of the soma-specific transcriptome by Polycomb-repressive complex 2 promotes male germ cell development.

Authors:  Weipeng Mu; Joshua Starmer; Andrew M Fedoriw; Della Yee; Terry Magnuson
Journal:  Genes Dev       Date:  2014-09-15       Impact factor: 11.361

Review 5.  Accessorizing and anchoring the LINC complex for multifunctionality.

Authors:  Wakam Chang; Howard J Worman; Gregg G Gundersen
Journal:  J Cell Biol       Date:  2015-01-05       Impact factor: 10.539

6.  Transient and Partial Nuclear Lamina Disruption Promotes Chromosome Movement in Early Meiotic Prophase.

Authors:  Jana Link; Dimitra Paouneskou; Maria Velkova; Anahita Daryabeigi; Triin Laos; Sara Labella; Consuelo Barroso; Sarai Pacheco Piñol; Alex Montoya; Holger Kramer; Alexander Woglar; Antoine Baudrimont; Sebastian Mathias Markert; Christian Stigloher; Enrique Martinez-Perez; Alexander Dammermann; Manfred Alsheimer; Monique Zetka; Verena Jantsch
Journal:  Dev Cell       Date:  2018-04-23       Impact factor: 12.270

7.  Expression of lamin C2 in mammalian oocytes.

Authors:  Marketa Koncicka; Jakub Cervenka; Daniel Jahn; Rita Sucha; Petr Vodicka; Ahmed Gad; Manfred Alsheimer; Andrej Susor
Journal:  PLoS One       Date:  2020-04-28       Impact factor: 3.240

8.  FBXO47 regulates telomere-inner nuclear envelope integration by stabilizing TRF2 during meiosis.

Authors:  Rong Hua; Huafang Wei; Chao Liu; Yue Zhang; Siyu Liu; Yueshuai Guo; Yiqiang Cui; Xin Zhang; Xuejiang Guo; Wei Li; Mingxi Liu
Journal:  Nucleic Acids Res       Date:  2019-12-16       Impact factor: 16.971

9.  The meiotic nuclear lamina regulates chromosome dynamics and promotes efficient homologous recombination in the mouse.

Authors:  Jana Link; Daniel Jahn; Johannes Schmitt; Eva Göb; Johannes Baar; Sagrario Ortega; Ricardo Benavente; Manfred Alsheimer
Journal:  PLoS Genet       Date:  2013-01-31       Impact factor: 5.917

10.  The impact of entropy on the spatial organization of synaptonemal complexes within the cell nucleus.

Authors:  Miriam Fritsche; Laura G Reinholdt; Mark Lessard; Mary Ann Handel; Jörg Bewersdorf; Dieter W Heermann
Journal:  PLoS One       Date:  2012-05-04       Impact factor: 3.240

  10 in total

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